Abstracts

Out of the 7,000 extant species of echinoderms, over 150 bioluminescent species have been identified to date. Among the five echinoderm classes, one class, the ophiuroids (brittle stars) dominate with 50% of the known bioluminescent species. The species Amphiura filiformis, commonly found buried in the muddy sediments of European seas, has been the subject of extensive study for over 30 years. Only two arms are extending outside the sediments when feeding on plankton and particulate organic matter. When mechanically stimulated, A. filiformis emits blue light at the arm spine level via a Renilla-like luciferase. However, our understanding of the luminescence triggering mechanism is limited to the nervous cholinergic control, while the biochemical and mechanical factors controlling its bioluminescence remain incompletely explored. The multidisciplinary approach of this study, which combines molecular biology and functional morphology, unveils a multi-level bioluminescence control. In silico analyses conducted on the recent reference chromosome-scale genome revealed the presence of at least 9 genes encoding Renilla luciferase-like proteins. Results from in situ hybridization suggest the involvement of several of these genes in bioluminescence, as indicated by their expression in the brittle star spines. From a cellular perspective, it is known that the light-producing cells are located at the base of the spine. Conversely, light emission is only visible at the tip of the spine, a duality that has remained rather enigmatic until now. Through histological and ultrastructural analysis, a light-guiding role is proposed for a pigmented sheath, potentially facilitating light transmission along the spine. Electron microscopy also revealed that different morphotypes of ciliated projections, known as stäbchens, are observed on the spine surface of A. filiformis, closely associated with the photocyte processes. In addition, luminometric tests show a luminescent response to conditioned water with chopped arms that mimic injured congeners. Given that stäbchens are generally considered as mechanoreceptors or chemoreceptors, these structures could therefore be involved in the light response of this luminous species to predator contact and/or conspecific chemical alarms signals. This study enhances our morpho-functional understanding of bioluminescence in A. filiformis, and also provides new insights into accessory structures, such as ciliated receptors or pigment cells, which may be linked to bioluminescence control in luminous ophiuroids.